scholarly journals The Role of Intact Frontostriatal Circuits in Error Processing

2006 ◽  
Vol 18 (4) ◽  
pp. 651-664 ◽  
Author(s):  
Markus Ullsperger ◽  
D. Yves von Cramon

The basal ganglia have been suggested to play a key role in performance monitoring and resulting behavioral adjustments. It is assumed that the integration of prefrontal and motor cortico—striato—thalamo—cortical circuits provides contextual information to the motor anterior cingulate cortex regions to enable their function in performance monitoring. So far, direct evidence is missing, however. We addressed the involvement of frontostriatal circuits in performance monitoring by collecting event-related brain potentials (ERPs) and behavioral data in nine patients with focal basal ganglia lesions and seven patients with lateral prefrontal cortex lesions while they performed a flanker task. In both patient groups, the amplitude of the error-related negativity was reduced, diminishing the difference to the ERPs on correct responses. Despite these electrophysiological abnormalities, most of the patients were able to correct errors. Only in lateral prefrontal cortex patients whose lesions extended into the frontal white matter, disrupting the connections to the motor anterior cingulate cortex and the striatum, were error corrections severely impaired. In sum, the fronto—striato—thalamo—cortical circuits seem necessary for the generation of error-related negativity, even when brain plasticity has resulted in behavioral compensation of the damage. Thus, error-related ERPs in patients provide a sensitive measure of the integrity of the performance monitoring network.

Author(s):  
Benjamin Voloh ◽  
Mariann Oemisch ◽  
Thilo Womelsdorf

AbstractThe prefrontal cortex and striatum form a recurrent network whose spiking activity encodes multiple types of learning-relevant information. This spike-encoded information is evident in average firing rates, but finer temporal coding might allow multiplexing and enhanced readout across the connected the network. We tested this hypothesis in the fronto-striatal network of nonhuman primates during reversal learning of feature values. We found that neurons encoding current choice outcomes, outcome prediction errors, and outcome history in their firing rates also carried significant information in their phase-of-firing at a 10-25 Hz beta frequency at which they synchronized across lateral prefrontal cortex, anterior cingulate cortex and striatum. The phase-of-firing code exceeded information that could be obtained from firing rates alone, was strong for inter-areal connections, and multiplexed information at three different phases of the beta cycle that were offset from the preferred spiking phase of neurons. Taken together, these findings document the multiplexing of three different types of information in the phase-of-firing at an interareally shared beta oscillation frequency during goal-directed behavior.HighlightsLateral prefrontal cortex, anterior cingulate cortex and striatum show phase-of-firing encoding for outcome, outcome history and reward prediction errors.Neurons with phase-of-firing code synchronize long-range at 10-25 Hz.Spike phases encoding reward prediction errors deviate from preferred synchronization phases.Anterior cingulate cortex neurons show strongest long-range effects.


2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Benjamin Voloh ◽  
Mariann Oemisch ◽  
Thilo Womelsdorf

Abstract The prefrontal cortex and striatum form a recurrent network whose spiking activity encodes multiple types of learning-relevant information. This spike-encoded information is evident in average firing rates, but finer temporal coding might allow multiplexing and enhanced readout across the connected network. We tested this hypothesis in the fronto-striatal network of nonhuman primates during reversal learning of feature values. We found that populations of neurons encoding choice outcomes, outcome prediction errors, and outcome history in their firing rates also carry significant information in their phase-of-firing at a 10–25 Hz band-limited beta frequency at which they synchronize across lateral prefrontal cortex, anterior cingulate cortex and anterior striatum when outcomes were processed. The phase-of-firing code exceeds information that can be obtained from firing rates alone and is evident for inter-areal connections between anterior cingulate cortex, lateral prefrontal cortex and anterior striatum. For the majority of connections, the phase-of-firing information gain is maximal at phases of the beta cycle that were offset from the preferred spiking phase of neurons. Taken together, these findings document enhanced information of three important learning variables at specific phases of firing in the beta cycle at an inter-areally shared beta oscillation frequency during goal-directed behavior.


2018 ◽  
Author(s):  
Mariann Oemisch ◽  
Stephanie Westendorff ◽  
Marzyeh Azimi ◽  
Seyed Ali Hassani ◽  
Salva Ardid ◽  
...  

SummaryPrediction errors signal unexpected outcomes indicating that expectations need to be adjusted. For adjusting expectations efficiently prediction errors need to be associated with the precise features that gave rise to the unexpected outcome. For many visual tasks this credit assignment proceeds in a multidimensional feature space that makes it ambiguous which object defining features are relevant. Here, we report of a potential solution by showing that neurons in all areas of the medial and lateral fronto-striatal networks encode prediction errors that are specific to separate features of attended multidimensional stimuli, with the most ubiquitous prediction error occurring for the reward relevant features. These feature specific prediction error signals (1) are different from a non-specific prediction error signal, (2) arise earliest in the anterior cingulate cortex and later in lateral prefrontal cortex, caudate and ventral striatum, and (3) contribute to feature-based stimulus selection after learning. These findings provide strong evidence for a widely-distributed feature-based eligibility trace that can be used to update synaptic weights for improved feature-based attention.HighlightsNeural reward prediction errors carry information for updating feature-based attention in all areas of the fronto-striatal network.Feature specific neural prediction errors emerge earliest in anterior cingulate cortex and later in lateral prefrontal cortex.Ventral striatum neurons encode feature specific surprise strongest for the goal-relevant feature.Neurons encoding feature-specific prediction errors contribute to attentional selection after learning.


2014 ◽  
Vol 111 (4) ◽  
pp. 787-803 ◽  
Author(s):  
Michael J. Koval ◽  
R. Matthew Hutchison ◽  
Stephen G. Lomber ◽  
Stefan Everling

The dorsolateral prefrontal cortex (dlPFC) and anterior cingulate cortex (ACC) have both been implicated in the cognitive control of saccadic eye movements by single neuron recording studies in nonhuman primates and functional imaging studies in humans, but their relative roles remain unclear. Here, we reversibly deactivated either dlPFC or ACC subregions in macaque monkeys while the animals performed randomly interleaved pro- and antisaccades. In addition, we explored the whole-brain functional connectivity of these two regions by applying a seed-based resting-state functional MRI analysis in a separate cohort of monkeys. We found that unilateral dlPFC deactivation had stronger behavioral effects on saccades than unilateral ACC deactivation, and that the dlPFC displayed stronger functional connectivity with frontoparietal areas than the ACC. We suggest that the dlPFC plays a more prominent role in the preparation of pro- and antisaccades than the ACC.


2015 ◽  
Vol 1 (4) ◽  
pp. 220-234 ◽  
Author(s):  
Peter M. Thompson ◽  
Dianne A. Cruz ◽  
Elizabeth A. Fucich ◽  
Dianna Y. Olukotun ◽  
Masami Takahashi ◽  
...  

2008 ◽  
Vol 99 (2) ◽  
pp. 759-772 ◽  
Author(s):  
Erik E. Emeric ◽  
Joshua W. Brown ◽  
Melanie Leslie ◽  
Pierre Pouget ◽  
Veit Stuphorn ◽  
...  

We describe intracranial local field potentials (LFP) recorded in the anterior cingulate cortex (ACC) of macaque monkeys performing a saccade countermanding task. The most prominent feature at ∼70% of sites was greater negative polarity after errors than after rewarded correct trials. This negative polarity was also evoked in unrewarded correct trials. The LFP evoked by the visual target was much less polarized, and the weak presaccadic modulation was insufficient to control the initiation of saccades. When saccades were cancelled, LFP modulation decreased slightly with the magnitude of response conflict that corresponds to the coactivation of gaze-shifting and -holding neurons estimated from the probability of canceling. However, response time adjustments on subsequent trials were not correlated with LFP polarity on individual trials. The results provide clear evidence that error- and feedback-related, but not conflict-related, signals are carried by the LFP in the macaque ACC. Finding performance monitoring field potentials in the ACC of macaque monkeys establishes a bridge between event-related potential and functional brain-imaging studies in humans and neurophysiology studies in non-human primates.


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